Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection
Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multi...
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description | Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. We investigated how the preinfection by freshwater pearl mussel Margaritifera margaritifera glochidia could influence the success of subsequent infection by the common trematode Diplostomum pseudospathaceum in brown trout Salmo trutta and vice versa whether preinfection by the trematode made fish more susceptible to glochidia infection. The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. Our study demonstrates how the timing and sequence of exposure to parasitic species can influence infection success in a host–multiparasite system. It indicates that the negative influence of glochidia on host fitness is likely to be underestimated and that this should be taken into consideration when organizing freshwater pearl mussel restoration procedures.
Freshwater pearl mussels's parasitic stage (glochidia) is usually considered to be not very harmful to their host, brown trout. However, even a small damage to fish gills caused by this parasite can make its host more vulnerable to subsequent infections. We demonstrate that the glochidia infection predispose fish to the infection by common trematode. Interestin |
doi_str_mv | 10.1002/ece3.4406 |
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Freshwater pearl mussels's parasitic stage (glochidia) is usually considered to be not very harmful to their host, brown trout. However, even a small damage to fish gills caused by this parasite can make its host more vulnerable to subsequent infections. We demonstrate that the glochidia infection predispose fish to the infection by common trematode. Interestingly, fish preinfected with trematode was also more vulnerable to infection with glochidia, but only, if preinfection happened shortly before the second infection.</description><identifier>ISSN: 2045-7758</identifier><identifier>EISSN: 2045-7758</identifier><identifier>DOI: 10.1002/ece3.4406</identifier><identifier>PMID: 30397441</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>community ecology ; Diplostomum ; experimental infection ; Exposure ; Fish ; Fitness ; freshwater pearl mussel ; Gills ; host–parasite interactions ; Infections ; Mollusks ; multiple infections ; Original Research ; Parasites ; Restoration ; Salmo trutta ; Species ; Trout ; Virulence</subject><ispartof>Ecology and evolution, 2018-10, Vol.8 (20), p.9986-9997</ispartof><rights>2018 The Authors. published by John Wiley & Sons Ltd.</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4436-4e4b53ff197d2d010bccba16a213ccaf11fdb8d34d3c1101b39ddba079fd67d3</citedby><cites>FETCH-LOGICAL-c4436-4e4b53ff197d2d010bccba16a213ccaf11fdb8d34d3c1101b39ddba079fd67d3</cites><orcidid>0000-0002-1525-6557</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206180/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206180/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11541,27901,27902,45550,45551,46027,46451,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30397441$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gopko, Mikhail</creatorcontrib><creatorcontrib>Chowdhury, M. Motiur R.</creatorcontrib><creatorcontrib>Taskinen, Jouni</creatorcontrib><title>Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection</title><title>Ecology and evolution</title><addtitle>Ecol Evol</addtitle><description>Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. We investigated how the preinfection by freshwater pearl mussel Margaritifera margaritifera glochidia could influence the success of subsequent infection by the common trematode Diplostomum pseudospathaceum in brown trout Salmo trutta and vice versa whether preinfection by the trematode made fish more susceptible to glochidia infection. The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. Our study demonstrates how the timing and sequence of exposure to parasitic species can influence infection success in a host–multiparasite system. It indicates that the negative influence of glochidia on host fitness is likely to be underestimated and that this should be taken into consideration when organizing freshwater pearl mussel restoration procedures.
Freshwater pearl mussels's parasitic stage (glochidia) is usually considered to be not very harmful to their host, brown trout. However, even a small damage to fish gills caused by this parasite can make its host more vulnerable to subsequent infections. We demonstrate that the glochidia infection predispose fish to the infection by common trematode. Interestingly, fish preinfected with trematode was also more vulnerable to infection with glochidia, but only, if preinfection happened shortly before the second infection.</description><subject>community ecology</subject><subject>Diplostomum</subject><subject>experimental infection</subject><subject>Exposure</subject><subject>Fish</subject><subject>Fitness</subject><subject>freshwater pearl mussel</subject><subject>Gills</subject><subject>host–parasite interactions</subject><subject>Infections</subject><subject>Mollusks</subject><subject>multiple infections</subject><subject>Original Research</subject><subject>Parasites</subject><subject>Restoration</subject><subject>Salmo trutta</subject><subject>Species</subject><subject>Trout</subject><subject>Virulence</subject><issn>2045-7758</issn><issn>2045-7758</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kctKAzEUhoMoKurCF5ABN3ZRPZlkZloXgpR6AcGFrg25nOjINKlJxuLbm1oVFcwmt-98nMNPyD6FYwpQnqBGdsw51GtkuwReDZumGq3_OG-RvRifIa8aSg7NJtliwMYN53SbPFy7hEHq1HoXC4VpgeiKtPDFXAYZ24Sx8LZQwS_yc_B9Ko7uZDfz-dKnJAenxSRX4kuPTq_YecDWWfxQ7pINK7uIe5_7Drm_mN5ProY3t5fXk_Oboeac1UOOXFXMWjpuTGmAgtJaSVrLkjKtpaXUGjUyjBumKQWq2NgYJaEZW1M3hu2Qs5V23qsZGo0uBdmJeWhnMrwJL1vx-8e1T-LRv4q6hJqOIAuOPgXB51FiErM2auw66dD3UeQ-gEHd8Cqjh3_QZ98Hl6fLVMVLzqqKZ2qwonTwMQa0381QEMvcxDI3scwtswc_u_8mv1LKwMkKWLQdvv1vEtPJlH0o3wG4AaNy</recordid><startdate>201810</startdate><enddate>201810</enddate><creator>Gopko, Mikhail</creator><creator>Chowdhury, M. Motiur R.</creator><creator>Taskinen, Jouni</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7X2</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1525-6557</orcidid></search><sort><creationdate>201810</creationdate><title>Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection</title><author>Gopko, Mikhail ; Chowdhury, M. 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Motiur R.</creatorcontrib><creatorcontrib>Taskinen, Jouni</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Ecology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gopko, Mikhail</au><au>Chowdhury, M. Motiur R.</au><au>Taskinen, Jouni</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection</atitle><jtitle>Ecology and evolution</jtitle><addtitle>Ecol Evol</addtitle><date>2018-10</date><risdate>2018</risdate><volume>8</volume><issue>20</issue><spage>9986</spage><epage>9997</epage><pages>9986-9997</pages><issn>2045-7758</issn><eissn>2045-7758</eissn><abstract>Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. We investigated how the preinfection by freshwater pearl mussel Margaritifera margaritifera glochidia could influence the success of subsequent infection by the common trematode Diplostomum pseudospathaceum in brown trout Salmo trutta and vice versa whether preinfection by the trematode made fish more susceptible to glochidia infection. The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. Our study demonstrates how the timing and sequence of exposure to parasitic species can influence infection success in a host–multiparasite system. It indicates that the negative influence of glochidia on host fitness is likely to be underestimated and that this should be taken into consideration when organizing freshwater pearl mussel restoration procedures.
Freshwater pearl mussels's parasitic stage (glochidia) is usually considered to be not very harmful to their host, brown trout. However, even a small damage to fish gills caused by this parasite can make its host more vulnerable to subsequent infections. We demonstrate that the glochidia infection predispose fish to the infection by common trematode. Interestingly, fish preinfected with trematode was also more vulnerable to infection with glochidia, but only, if preinfection happened shortly before the second infection.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>30397441</pmid><doi>10.1002/ece3.4406</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-1525-6557</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | community ecology Diplostomum experimental infection Exposure Fish Fitness freshwater pearl mussel Gills host–parasite interactions Infections Mollusks multiple infections Original Research Parasites Restoration Salmo trutta Species Trout Virulence |
title | Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection |
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